Data from: Comparative developmental transcriptomics reveals rewiring of a highly conserved gene regulatory network during a major life history switch in the sea urchin genus Heliocidaris

The ecologically significant shift in developmental strategy from planktotrophic (feeding) to lecithotrophic (nonfeeding) development in the sea urchin genus Heliocidaris is one of the most comprehensively studied life history transitions in any animal. Although the evolution of lecithotrophy involved substantial changes to larval development and morphology, it is not known to what extent changes in gene expression underlie the developmental differences between species, nor do we understand how these changes evolved within the context of the well-defined gene regulatory network (GRN) underlying sea urchin development. To address these questions, we used RNA-seq to measure expression dynamics across development in three species: the lecithotroph Heliocidaris erythrogramma, the closely related planktotroph H. tuberculata, and an outgroup planktotroph Lytechinus variegatus. Using well-established statistical methods, we developed a novel framework for identifying, quantifying, and polarizing evolutionary changes in gene expression profiles across the transcriptome and within the GRN. We found that major changes in gene expression profiles were more numerous during the evolution of lecithotrophy than during the persistence of planktotrophy, and that genes with derived expression profiles in the lecithotroph displayed specific characteristics as a group that are consistent with the dramatically altered developmental program in this species. Compared to the transcriptome, changes in gene expression profiles within the GRN were even more pronounced in the lecithotroph. We found evidence for conservation and likely divergence of particular GRN regulatory interactions in the lecithotroph, as well as significant changes in the expression of genes with known roles in larval skeletogenesis. We further use coexpression analysis to identify genes of unknown function that may contribute to both conserved and derived developmental traits between species. Collectively, our results indicate that distinct evolutionary processes operate on gene expression during periods of life history conservation and periods of life history divergence, and that this contrast is even more pronounced within the GRN than across the transcriptome as a whole.

海胆属（Heliocidaris）中，发育策略从浮游摄食型（planktotrophic，即依赖摄食）向卵黄营养型（lecithotrophic，即非依赖摄食）的具有重要生态意义的转变，是所有动物类群中研究最为透彻的生活史转变之一。尽管卵黄营养型的演化伴随幼体发育与形态的显著改变，目前仍不清楚物种间的发育差异在多大程度上由基因表达变化所介导，同时我们也尚不明确，这些变化是如何在海胆发育所依托的经典基因调控网络（gene regulatory network, GRN）框架下发生演化的。为解答这些问题，我们通过RNA测序（RNA-seq）对三个物种的全发育过程的表达动态进行了定量检测：卵黄营养型物种Heliocidaris erythrogramma、亲缘关系紧密的浮游摄食型物种H. tuberculata，以及外类群浮游摄食型物种Lytechinus variegatus。我们依托成熟的统计学方法，构建了一套全新的分析框架，用于在转录组（transcriptome）层面以及基因调控网络内部，对基因表达谱的演化改变进行识别、量化并标定其演化方向。我们发现，在卵黄营养型的演化过程中，基因表达谱的重大改变数量远多于浮游摄食型发育维持保守的阶段；同时，该卵黄营养型物种中具有衍生表达谱的基因，作为一个整体呈现出特定特征，与该物种显著重塑的发育程序相符。相较于整个转录组，该卵黄营养型物种的基因调控网络内部的基因表达谱改变更为显著。我们发现了该物种中基因调控网络特定调控交互作用的保守性与潜在分化的证据，同时也发现了已知参与幼虫骨骼发生（larval skeletogenesis）的基因的表达发生了显著改变。我们进一步通过共表达分析（coexpression analysis），筛选出了一批功能未知的基因，这些基因可能参与了物种间保守以及衍生的发育性状。综上，我们的研究结果表明，在生活史保守与生活史分化的不同时期，不同的演化过程作用于基因表达层面，且这种差异在基因调控网络内部比在整个转录组层面更为显著。